Unraveling the mystery of a myxozoan parasite of the trout: redescription of Chloromyxum schurovi

. 2024 Sep 04 ; 71 () : . [epub] 20240904

Jazyk angličtina Země Česko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39301677

Myxozoans are microscopical parasites widely distributed in fish, with over 2,600 described species, but their actual diversity is still underestimated. Among salmonids, more than 70 myxozoan species have been identified. This study focuses on species of Chloromyxum Mingazzini, 1890 that infect salmonid kidneys, particularly C. majori Yasutake et Wood, 1957 and C. schurovi Shulman et Ieshko, 2003. Despite their similar spore morphology, they exhibit distinct host preferences, tissue affinities and geographical distributions. Chloromyxum schurovi predominantly infects the renal tubules of Salmo salar Linnaues and S. trutta Linnaeus in Europe, while C. majori targets the glomeruli of Oncorhynchus mykiss (Walbaum) and O. tshawytscha (Walbaum) in North America. The sequence data for C. majori and C. schurovi have been either missing or questionable. In our study, we examined the kidneys of two salmonid species for chloromyxid infections, using both morphological and molecular data to characterise Chloromyxum species in salmonids. The sequence of C. schurovi obtained in our study did not match the previously published parasite data. Instead, it clustered as an independent lineage sister to the Paramyxidium Freeman et Kristmundsson, 2018 clade gathering the species from various fish organs, including the urinary tract. Our findings clarified the taxonomic origin of the previous C. schurovi sequence as Myxidium giardi Cépède, 1906, highlighting the risks associated with the presence of myxozoan blood stages in the bloodstream of their fish host and the challenges of non-specific PCR amplification. We redescribe C. schurovi, thus contributing to a better understanding of the diversity and phylogeny of kidney-infecting species of Chloromyxum.

Zobrazit více v PubMed

Atkinson S.D., Bartošová-Sojková P., Whipps C.M., Bartholomew J.L. 2015: Approaches for characterising myxozoan species. In: B. Okamura, A. Gruhl and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 111-123. DOI

Bartholomew J.L., Alexander J.D., Hallett S.L., Alama-Bermejo G., Atkinson S.D. 2022: Ceratonova shasta: a cnidarian parasite of annelids and salmonids. Parasitology 149: 1862-1875. PubMed DOI

Bartošová P., Fiala I. 2011: Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol. Res. 108: 573-583. PubMed DOI

Bartošová-Sojková P., Hrabcová M., Pecková H., Patra S., Kodádková A., Jurajda P., Tyml T., Holzer A.S. 2014: Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. Int. J. Parasitol. 44: 565-577. PubMed DOI

Bartošová-Sojková P., Lövy A., Reed C.C., Lisnerová M., Tomková T., Holzer A.S., Fiala, I. 2018: Life in a rock pool: radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces. PLoS One 13: e0194042 PubMed DOI

Buchmann K., Bresciani J. 1997: Parasitic infections in pond-reared rainbow trout Oncorhynchus mykiss in Denmark. Dis. Aquat. Org. 28: 125-138. DOI

Cantatore D.M.P., Irigoitia M.M., Holzer A.S., Bartošová-Sojková P., Pecková H., Fiala I., Timi J.T. 2018: The description of two new species of Chloromyxum from skates in the Argentine Sea reveals that a limited geographic host distribution causes phylogenetic lineage separation of myxozoans in Chondrichthyes. Parasite 25: 47. PubMed DOI

Davis H.S. 1944: A revision of the genus Henneguya (Myxosporidia) with descriptions of two new species. Trans. Am. Microsc. Soc. 63: 311-320. DOI

Dorucu M., Crompton D.W.T., Huntingford F.A., Walter D.W. 1995: The ecology of endoparasitic helminth infections of brown trout (Salmo trutta) and rainbow trout (Oncorhynchus mykiss) in Scotland. Folia Parasitol. 42: 29-36.

Eiras J.C. 2002: Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst. Parasitol. 52: 43-54. PubMed DOI

Eiras J.C., Lu Y.S., Gibson D.I., Fiala I., Saraiva A., Cruz C., Santos M.J. 2012: Synopsis of the species of Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea: Chloromyxidae). Syst. Parasitol. 83: 203-225. PubMed DOI

Eiras J.C., Saraiva A., Cruz C. 2014: Synopsis of the species of Kudoa Meglitsch, 1947 (Myxozoa: Myxosporea: Multivalvulida). Syst. Parasitol. 87: 153-180. PubMed DOI

Eiras J.C., Saraiva A., Cruz C.F., Santos M.J., Fiala I. 2011: Synopsis of the species of Myxidium Bütschli, 1882 (Myxozoa: Myxosporea: Bivalvulida). Syst. Parasitol. 80: 81-116. PubMed DOI

English C.J., Tyml T., Botwright N.A., Barnes A.C., Wynne J.W., Lima P.C., Cook M.T. 2019: A diversity of amoebae colonise the gills of farmed Atlantic salmon (Salmo salar) with amoebic gill disease (AGD). Eur. J. Protistol. 67: 27-45. PubMed DOI

Eszterbauer E., Atkinson S., Diamant A., Morris D., El-Matbouli M., Hartikainen H. 2015: Myxozoan life cycles: practical approaches and insights. In: B. Okamura, A. Gruhl and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 175-198. DOI

Feist S.W., Peeler E.J., Gardiner R., Smith E., Longshaw M. 2002: Proliferative kidney disease and renal myxosporidiosis in juvenile salmonids from rivers in England and Wales. J. Fish Dis. 25: 451-458. DOI

Fiala I. 2006: The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int. J. Parasitol. 36: 1521-1534. PubMed DOI

Fiala I., Bartošová-Sojková P., Whipps C.M. 2015: Classification and phylogenetics of Myxozoa. In: B. Okamura, A. Gruhl and J.L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, pp. 85-110. DOI

Fiala I., Dyková I. 2004: The phylogeny of marine and freshwater species of the genus Chloromyxum Mingazzini, 1890 (Myxosporea: Bivalvulida) based on small subunit ribosomal RNA gene sequences. Folia Parasitol. 51: 211-214. DOI

Freeman M.A., Kristmundsson Á. 2018: Studies of Myxidium giardi Cépède, 1906 infections in Icelandic eels identifies a genetically diverse clade of myxosporeans that represents the Paramyxidium n. g. (Myxosporea: Myxidiidae). Parasit. Vectors 11: 1-13. PubMed DOI

Froese R., Pauly D. (Eds.) 2024: FishBase. World Wide Web electronic publication. www.fishbase.org, version (1/2024).

Gleeson R.J., Adlard R.D. 2012: Phylogenetic relationships amongst Chloromyxum Mingazzini, 1890 (Myxozoa: Myxosporea), and the description of six novel species from Australian elasmobranchs. Parasitol. Int. 61: 267-274. PubMed DOI

Grossel G., Handlinger J., Battaglene S., Munday B. 2005: Diagnostic polymerase chain reaction assay to detect Kudoa neurophila (Myxozoa: Multivalvulida) in a marine finfish hatchery. Dis. Aquat. Org. 64: 141-149. PubMed DOI

Hartikainen H., Bass D., Briscoe A.G., Knipe H., Green A.J., Okamura B. 2016: Assessing myxozoan presence and diversity using environmental DNA. Int. J. Parasitol. 46: 781-792. PubMed DOI

Hillis D.M. 1998: Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 47: 3-8. PubMed DOI

Hillis D.M., Dixon M.T. 1991: Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 66: 411-453. PubMed DOI

Holzer A.S. 2004: Molecular studies on Sphaerospora truttae and other freshwater myxozoans. PhD Thesis, University of Stirling, Stirling, UK, 260 pp.

Holzer A.S., Bartošová P., Pecková H., Tyml T., Atkinson S., Bartholomew J., Sipos D., Eszterbauer E., Dyková, I. 2013: 'Who's who' in renal sphaerosporids (Bivalvulida: Myxozoa) from common carp, Prussian carp and goldfish - molecular identification of cryptic species, blood stages and new members of Sphaerospora sensu stricto. Parasitology 140: 46-60. PubMed DOI

Holzer A.S., Hartigan A., Patra S., Pecková H., Eszterbauer E. 2014: Molecular fingerprinting of the myxozoan community in common carp suffering Swim Bladder Inflammation (SBI) identifies multiple etiological agents. Parasit. Vectors 7: 1-9. PubMed DOI

Holzer A.S., Sommerville C., Wootten R. 2004: Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int. J. Parasitol. 34: 1099-1111. PubMed DOI

Holzer A.S., Sommerville C., Wootten R. 2006a: Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shulman & Ieshko 2003. Parasitol. Res. 99: 90-96. PubMed DOI

Holzer A.S., Sommerville C., Wootten R. 2006b: Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L. Parasitol. 132: 193-205. PubMed DOI

Jirků M., Bartošová P., Kodádková A., Mutschmann F. 2011: Another chloromyxid lineage: molecular phylogeny and redescription of Chloromyxum careni from the Asian horned frog Megophrys nasuta. J. Euk. Microbiol. 58: 50-59. PubMed DOI

Katoh K., Kuma K.I., Toh H., Miyata T. 2005: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl, Acids Res. 33: 511-518. PubMed DOI

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P., Drummond A. 2012: Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. PubMed DOI

Korytář T., Wiegertjes G.F., Zusková E., Tomanová A., Lisnerová M., Patra S., Sieranski V., Šíma R., Born-Torrijos A., Wentzel A.S., Blasco-Monleon S., Yanes-Roca C., Policar T., Holzer A.S. 2019: The kinetics of cellular and humoral immune responses of common carp to presporogonic development of the myxozoan Sphaerospora molnari. Parasit. Vectors 12: 1-16. PubMed DOI

Lisnerová M., Bartošová-Sojková P., Lövy A., Blabolil P., Fiala I. 2024: Evidence of striking morphological similarity and tissue tropism of phylogenetically distant myxozoan genera: Myxidium and Paramyxidium in the kidney of the European eel. Folia Parasitol. 71: 013. PubMed DOI

Lisnerová M., Blabolil P., Holzer A., Jurajda P., Fiala I. 2020: Myxozoan hidden diversity: the case of Myxobolus pseudodispar Gorbunova, 1936. Folia Parasitol. 67: 019. PubMed DOI

Lisnerová M., Holzer A., Blabolil P., Fiala I. 2023: Evaluation and optimization of an eDNA metabarcoding assay for detection of freshwater myxozoan communities. Environ. DNA 5: 312-325. DOI

Lisnerová M., Martinek I.N., Alama-Bermejo G., Bouberlová K., Schaeffner B.C., Nkabi N., Holzer A.S., Bartošová-Sojková P. 2022: An ancient alliance: matching evolutionary patterns of cartilaginous fishes (Elasmobranchii) and chloromyxid parasites (Myxozoa). Infect. Genet. Evol. 103: 105346. PubMed DOI

Lom J., Arthur J.R. 1989: A guideline for the preparation of species descriptions in Myxosporea. J. Fish Dis. 12: 151-156. DOI

Lom J., Dyková I. 1993: Scanning electron microscopic revision of common species of the genus Chloromyxum (Myxozoa: Myxosporea) infecting European freshwater fishes. Folia Parasitol. 40: 161-174.

Lom J., Dyková, I. 2006: Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 53: 1-36. DOI

Malmberg G., Collins C.M., Cunningham C.O., Jalali B.J. 2007: Gyrodactylus derjavinoides sp. nov. (Monogenea, Platyhelminthes) on Salmo trutta trutta L. and G. derjavini Mikailov, 1975 on S. t. caspius Kessler, two different species of Gyrodactylus-combined morphological and molecular investigations. Acta Parasitol. 52: 89-103. DOI

Molnár K. 2007: Site preference of myxozoans in the kidneys of Hungarian fishes. Dis. Aquat. Org. 78: 45-53. PubMed DOI

Moravec F. 2003: Observations on the metazoan parasites of the Atlantic salmon (Salmo salar) after its reintroduction into the Elbe River basin in the Czech Republic. Folia Parasitol. 50: 298-304. PubMed DOI

Nakajima K., Egusa S. 1975: Pseudorhadinorhynchus samegaiensis n. sp. (Acanthocephala), from cultured rainbow trout, Salmo gairdnerii in Japan. Fish Pathol. 10: 58-68. DOI

Nylund A., Karlsbakk E., Saether P.A., Koren C., Larsen T., Nielsen B.D., Brøderud A.E., Høstlund C., Fjellsøy K.R., Lervik K., Rosnes L. 2005: Parvicapsula pseudobranchicola (Myxosporea) in farmed Atlantic salmon Salmo salar: tissue distribution, diagnosis and phylogeny. Dis. Aquat. Org. 63: 197-204. PubMed DOI

Nylund S., Nylund A.R.E., Watanabe K., Arnesen C.E., Karlsbakk E. 2010: Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). J. Euk.. Microbiol. 57: 95-114. PubMed DOI

Okamura B., Hartigan A., Naldoni J. 2018: Extensive uncharted biodiversity: the parasite dimension. Integr. Comp. Biol. 58: 1132-1145. PubMed DOI

Posada D. 2008: jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256. PubMed DOI

Schell S.C. 1974: The life history of Sanguinicola idahoensis sp. n. (Trematoda: Sanguinicolidae), a blood parasite of steelhead trout, Salmo gairdneri Richardson. J. Parasitol. 561-566. DOI

Schneider C.A., Rasband W.S., Eliceiri K.W. 2012: NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9: 671-675. PubMed DOI

Sedlaczek J. 1991: Chloromyxum sp. (Myxosporidia) in the kidney of Salmo trutta f. fario (Osteichthyes). Angew. Parasitol. 32: 137-142.

Shulman B.S., Ieshko E.P. 2003: Chloromyxum schurovi sp. n. - new species of myxosporidia (Myxosporea: Sphaerosporidae) of salmon fish (Salmonidae). Parasitology 37: 246-247.

Shulman S.S. 1966: [Myxosporidia of the USSR.] Nauka, Moscow-Leningrad, 504 pp. (In Russian.)

Stamatakis A. 2006: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. PubMed DOI

Sudhagar A., Kumar G., El-Matbouli M. 2019: The malacosporean myxozoan parasite Tetracapsuloides bryosalmonae: a threat to wild salmonids. Pathogens 9: 16. PubMed DOI

Vollset K.W., Halttunen E., Finstad B., Karlsen Ø., Bjørn P.A., Dohoo I. 2017: Salmon lice infestations on sea trout predicts infestations on migrating salmon post-smolts. ICES J. Mar. Sci. 74: 2354-2363. DOI

Whipps C.M., Adlard R.D., Bryant M.S., Lester R.J., Findlav V., Kent M.L. 2003: First report of three Kudoa species from eastern Australia: Kudoa thyrsites from mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). J. Appl. Microbiol. 50: 215-219. PubMed DOI

Woo P.T.K., Li S. 1990: In vitro attenuation of Cryptobia salmositica and its use as a live vaccine against cryptobiosis in Oncorhynchus mykiss. J. Parasitol. 78: 752-755. DOI

Wootten R., Smith J.W. 1980: Studies on the parasite fauna of juvenile Atlantic salmon, Salmo salar L., cultured in fresh water in eastern Scotland. Z. Parasitenkd. 63: 221-231. PubMed DOI

Yasutake W.T., Wood E.M. 1957: Some myxosporidia found in Pacific Northwest salmonids. J. Parasitol. 43: 633-642. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...